Abstract
Entotympanics are independent elements present in the auditory bullae of various eutherians. An entotympanic has been reported for extant pangolins of the Order Pholidota, but the actual distribution of this element remains uncertain, in part, because it is a small, loosely attached structure that is often lost in macerated skulls. Consequently, it is unknown whether or not the entotympanic characterizes Pholidota primitively or has evolved within the group. This report addresses the morphology and distribution of the entotympanic among living and extinct pholidotans. An entotympanic occurs in the African pangolins Manis gigantea, M. temminckii, and in one specimen of M. tricuspis. In each, it is a small, nodular bone that occupies a distinct fossa primarily on the basioccipital, the presence of which allows us to assess the occurrence of an entotympanic even in specimens in which the bone has fallen out. Both the entotympanic and the basioccipital facet are lacking in the four remaining extant pangolin species and in the late Eocene pangolin Patriomanis. To assess the significance of this entotympanic distribution, a phylogenetic analysis of extant pangolins plus Patriomanis based on 67 cranial characters was performed. Four different outgroup analyses all resulted in the same single most parsimonious tree, in which the three extant Asian pangolins form a monophyletic clade and the four extant African pangolins fall into a paraphyletic assemblage. Optimization of the entotympanic distribution onto this tree results in two patterns, dependent on the outgroup choice. If Patriomanis is the sole outgroup to the extant pangolins, the entotympanic arises within pangolins as a synapomorphy of Manis gigantea and M. temminckii, convergently acquired in some M. tricuspis. If Xenarthra and Palaeanodonta are employed as outgroups, the entotympanic optimization is ambiguous: the pattern is either as above or the entotympanic is present primitively within Pholidota and lost secondarily in Patriomanis and a clade comprising M. tricuspis, M. tetradactyla, and the Asian forms.
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LITERATURE CITED
Barlow, J. C. (1984). Xenarthrans and pholidotes. In: Orders and Families of Recent Mammals of the World, S. Anderson and J. Knox Jones, Jr., eds., pp. 219–239, John Wiley & Sons, New York.
Cifelli, R. L. (1983). Eutherian tarsals from the late Paleocene of Brazil. Am. Mus. Novitates 2761: 1–31.
Corbet, G. B., and Hill, J. E. (1991). A World List of Mammalian Species, 3rd ed., British Museum (Natural History), London.
Czelusniak, J., Goodman, M., Koop, B. F., Tagle, D. A., Shoshani, J., Braunitzer, G., Kleinschmidt, T. K., DeJong, W. W., and Matsuda, G. (1990). Perspectives from amino acid and nucleotide sequences on cladistic relationships among higher taxa of Eutheria. In: Current Mammalogy, Vol. 2, H. H. Genoways, ed., pp. 545–572, Plenum Press, New York.
De Beer, G. R. (1937). The Development of the Vertebrate Skull, Clarendon Press, Oxford.
Emry, R. J. (1970). A North American Oligocene pangolin and other additions to the Pholidota. Bull. Am. Mus. Nat. Hist. 142: 455–510.
Engelmann, G. F. (1978). The Logic of Phylogenetic Analysis and the Phylogeny of the Xenarthra (Mammalia), Ph.D. dissertation, Columbia University, New York.
Engelmann, G. F. (1985). The phylogeny of the Xenarthra. In: The Ecology and Evolution of Armadillos, Sloths, and Vermilinguas, G. G. Montgomery, ed., pp. 51–64, Smithsonian Institution Press, Washington, DC.
Eschweiler, R. (1899). Zur vergleichenden Anatomie der Muskeln und der Topographie des Mittelohres verschiedener Säugethiere. Arch. Mikr. Anat. 53: 558–622.
Frechkop, S. (1931). Notes sur les mammifères. VI. Quelques observations sur la classification des pangolins (Manidae). Bull. Mus. Roy. Sci. Nat. Belg. 7: 1–14.
Gaudin, T. J. (1993). Phylogeny of the Tardigrada (Mammalia, Xenarthra) and the Evolution of Locomotor Function in the Xenarthra, Ph.D. dissertation, University of Chicago, Chicago.
Gaudin, T. J. (1995). The ear region of edentates and the phylogeny of the Tardigrada (Mammalia, Xenarthra). J. Vert. Paleontol. 15: 672–705.
Gaudin, T. J., and Branham, D. G. (1998). The phylogeny of the Myrmecophagidae (Mammalia, Xenarthra, Vermilingua) and the relationship of Eurotamandua to the Vermilingua. J. Mammal. Evol. 5: 237–265.
Gaudin, T. J., Wible, J. R., Hopson, J. A., and Turnbull, W. D. (1996). Reexamination of the morphological evidence for the Cohort Epitheria (Mammalia, Eutheria). J. Mammal. Evol. 3: 31–79.
Glass, B. P. (1985). History of classification and nomenclature in Xenarthra (Edentata). In: The Ecology and Evolution of Armadillos, Sloths, and Vermilinguas, G. G. Montgomery, ed., pp. 1–3, Smithsonian Institution Press, Washington, DC.
Grassé, P.-P. (1955). Ordre de Pholidotes. In: Traité de Zoologie, Vol. 17, Mammifères, P.-P. Grassé, ed., pp. 1267–1282, Masson et Cie, Paris.
Graur, D., Duret, L., and Gouy, M. (1996). Phylogenetic position of the order Lagomorpha (rabbits, hares and allies). Nature 379: 333–335.
Hershkovitz, P. (1992). Ankle bones: The Chilean opposum Dromiciops gliroides Thomas, and marsupial phylogeny. Bonn. Zool. Beitr. 43: 181–213.
Hoffstetter, R. (1982). Les édentés xenartres, un groupe singulier de la faune neotropical. In: Paleontology, Essential of Historical Geology, E. M. Gallitelli, ed., pp. 385–443, STEM Mocchi Modena Press, Modena, Italy.
Jollie, M. (1968). The head skeleton of a new-born Manis javanica with comments on the ontogeny and phylogeny of the mammal head skeleton. Acta Zool. 49: 227–305.
Koenigswald, W. v., and Martin, T. (1990). Ein Skelett von Necromanis franconica, einem Schuppentier (Pholidota, Mammalia) aus dem Aquitan von Saulcet im Allier-Becken (Frankreich). Ecol. Geol. Helv. 83: 845–864.
MacPhee, R. D. E. (1979). Entotympanics, ontogeny and primates. Folia Primatol. 31: 23–47.
MacPhee, R. D. E. (1981). Auditory regions of primates and eutherian insectivores: Morphology, ontogeny and character analysis. Contrib. Primatol. 18: 1–282.
MacPhee, R. D. E. (1994). Morphology, adaptations, and relationships of Plesiorycteropus, and a diagnosis of a new order of eutherian mammals. Bull. Am. Mus. Nat. Hist. 220: 1–214.
MacPhee, R. D. E., and Novacek, M. J. (1993). Definition and relationships of Lipotyphla. In: Mammal Phylogeny: Placentals, F. S. Szalay, M. J. Novacek, and M. C. McKenna, eds., pp. 13–31, Springer-Verlag, New York.
Maier, W. (1989). Morphologische Untersuchungen am Mittelohr der Marsupialia. Z. Zool. Syst. Evol.-Forsch. 27: 149–168.
Matthew, W. D. (1918). A revision of the lower Eocene Wasatch and Wind River faunas. Part V. Insectivora (continued), Glires, Edentata. Bull. Am. Mus. Nat. Hist. 38: 565–657.
McKenna, M. C. (1992). The alpha crystallin A chain of the eye lens and mammalian phylogeny. Ann. Zool. Fenn. 28: 349–360.
McKenna, M. C., and Bell, S. K. (1997). Classification of Mammals Above the Species Level, Colombia University Press, New York.
Miyamoto, M. M., and Goodman, M. (1986). Biomolecular systematics of eutherian mammals: Phylogenetic pattern and classification. Syst. Zool. 35: 230–240.
Norman, J. E., and Ashley, M. V. (1994). Molecular systematics of the xenarthrans. Am. Soc. Mamm. 75th Anniv. Mtg., Abstr. 271.
Norris, C. A. (1993). Changes in the composition of the auditory bulla in southern Solomon Islands populations of the grey cuscus, Phalanger orientalis breviceps (Marsupialia, Phalangeridae). Zool. J. Linn. Soc. 107: 93–106.
Novacek, M. J. (1977). Aspects of the problem of variation, origin and evolution of the eutherian auditory bulla. Mammal Rev. 7: 131–149.
Novacek, M. J. (1986). The skull of leptictid insectivorans and the higher-level classification of eutherian mammals. Bull. Am. Mus. Nat. Hist. 183: 1–112.
Novacek, M. J. (1992). Mammalian phylogeny: Shaking the tree. Nature 356: 121–125.
Novacek, M. J. (1993). Patterns of diversity in the mammalian skull. In: The Skull, Vol. 2: Patterns of Structural and Systematic Diversity, J. Hanken and B. K. Hall, eds., pp. 438–545, University of Chicago Press, Chicago.
Novacek, M. J., and Wyss, A. (1986). Higher-level relationships of the recent eutherian orders: morphological evidence. Cladistics 2: 257–287.
Novacek, M. J., Wyss, A. R., and McKenna, M. C. (1988). The major groups of eutherian mammals. In: The Phylogeny and Classification of Tetrapods, Vol. 2. Mammals, M. J. Benton, ed., pp. 31–71, Clarendon Press, Oxford.
Nowak, R. M. (1991). Walker's Mammals of the World, 5th ed., Johns Hopkins University Press, Baltimore.
Patterson, B. (1978). Pholidota and Tubulidentata. In: Evolution of African Mammals, V. J. Maglio and H. B. S. Cooke, eds., pp. 268–278, Harvard University Press, Cambridge, MA.
Patterson, B., Segall, W., and Turnbull, W. D. (1989). The ear region in xenarthrans (=Edentata, Mammalia). Part I. Cingulates. Fieldiana Geol. n.s. 18: 1–46.
Patterson, B., Segall, W., Turnbull, W. D., and Gaudin, T. J. (1992). The ear region in xenarthrans (=Edentata, Mammalia). Part II. Pilosa (sloths, anteaters), palaeanodonts, and a miscellany. Fieldiana Geol. n.s. 24: 1–79.
Pocock, R. I. (1924). The external characters of the pangolins (Manidae). Proc. Zool. Soc. London 1924: 707–723.
Reiss, K. Z. (1996). Evolution of the feeding apparatus in ant-eating mammals: When do we stop believing in convergence? Am. Zool. 36(5): 85A.
Reiss, K. Z. (1997). Myology of the feeding apparatus of myrmecophagid anteaters (Xenarthra: Myrmecophagidae). J. Mammal. Evol. 4: 87–117.
Rose, K. D. (1979). A new Paleocene palaeanodont and the origin of the Metacheiromyidae (Mammalia). Breviora Mus. Comp. Zool. 455: 1–14.
Rose, K. D., and Emry, R. J. (1993). Relationships of Xenarthra, Pholidota, and fossil “edentates.” In: Mammal Phylogeny: Placentals, F. S. Szalay, M. J. Novacek, and M. C. McKenna, eds., pp. 81–102, Springer-Verlag, New York.
Sarich, V. M. (1985). Xenarthran systematics: albumin immunological evidence. In: The Evolution and Ecology of Armadillos, Sloths, and Vermilinguas, G. G. Montgomery, ed., pp. 77–81, Smithsonian Institution Press, Washington, DC.
Schlitter, D. A. (1993). Order Pholidota. In: Mammal Species of the World, D. E. Wilson and D. M. Reeder, eds., p. 415, Smithsonian Institution Press, Washington, DC.
Schneider, R. (1955). Zur Entwicklung des Chondrocraniums der Gattung Bradypus. Gegenbaurs Morph. Jb. 95: 209–301.
Segall, W. (1973). Characteristics of the ear, especially the middle ear in fossorial mammals, compared with those in the Manidae. Acta Anat. 86: 96–110.
Simpson, G. G. (1931). Metacheiromys and the relationships of the Edentata. Bull. Am. Mus. Nat. Hist. 59: 295–381.
Simpson, G. G. (1945). The principles of classification and a classification of mammals. Bull. Am. Mus. Nat. Hist. 85: 1–350.
Spatz, W. B. (1966). Zur Ontogenese der Bulla tympanica von Tupaia glis Diard 1820 (Prosimiae, Tupaiiformes). Folia Primatol. 4: 26–50.
Springer, M. S., Cleven, G. C., Madsen, O., de Jong, W. W., Waddell, V. G., Amrine, H. M., and Stanhope, M. J. (1997). Endemic African mammals shake the phylogenetic tree. Nature 388: 61–64.
Starck, D. (1941). Zur Morphologie des Primordialkraniums von Manis javanica Desm. Gegenbaurs Morph. Jb. 86: 1–122.
Storch, G. (1978). Eomanis waldi, ein Schuppentier aus dem Mittel-Eozän der “Grube Messel” bei Darmstadt (Mammalia: Pholidota). Senckenberg. lethaea 59: 503–529.
Storch, G., and Martin, T. (1994). Ecomanis krebsi, ein neues Schuppentier aus dem Mittel-Eozän der Grube Messel bei Darmstadt (Mammalia: Pholidota). Berliner geowiss. Abh. E13: 83–97.
Swofford, D. L. (1993). PAUP: Phylogenetic Analysis Using Parsimony, Version 3.1.1, Smithsonian Institution, Washington, DC.
Szalay, F. S. (1977). Phylogenetic relationships and a classification of eutherian Mammalia. In: Major Patterns in Vertebrate Evolution, M. K. Hecht, P. C. Goody, and B. M. Hecht, eds., pp. 315–374, Plenum Press, New York.
van Kampen, P. N. (1905). Die Tympanalgegend des Säugetiereschädels. Gegenbaurs Morph. Jb. 34: 321–722.
van Kampen, P. N. (1915). De Phylogenie van het entotympanicum. Tijdschr. Ned. Dierkd. Ver. 14: xxiv.
van der Klaauw, J. C. (1922). Über die Entwicklung des Entotympanicums. Tijdschr. Ned. Dierkd. Ver. 18: 135–174.
van der Klaauw, J. C. (1931). On the auditory bulla in some fossil mammals. Bull. Am. Mus. Nat. Hist. 62: 1–352.
Wible, J. R. (1984). The Ontogeny and Phylogeny of the Mammalian Cranial Arterial Pattern, Ph.D. dissertation, Duke University, Durham, NC.
Wible, J. R. (1986). Transformations in the extracranial course of the internal carotid artery in mammalian phylogeny. J. Vert. Paleontol. 6: 313–325.
Wible, J. R., and Martin, J. R. (1993). Ontogeny of the tympanic floor and roof in archontans. In: Primates and Their Relatives in Phylogenetic Perspective, R. D. E. MacPhee, ed., pp. 111–148, Plenum Press, New York.
Wible, J. R., and Novacek, M. J. (1988). Cranial evidence for the monophyletic origin of bats. Am. Mus. Novitates 2911: 1–19.
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Gaudin, T.J., Wible, J.R. The Entotympanic of Pangolins and the Phylogeny of the Pholidota (Mammalia). Journal of Mammalian Evolution 6, 39–65 (1999). https://doi.org/10.1023/A:1020538313412
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DOI: https://doi.org/10.1023/A:1020538313412